A Subpopulation of Mesencephalic Dopamine Neurons Interfaces the Shell of Nucleus Accumbens and the Dorsolateral Striatum in Rats

Nigrostriatal dopaminergic neurons are usually considered to interface the ventral limbic and dorsal sensorimotor striatum, since the shell of the nucleus accumbens (Acb shell) projects to the ventral tegmental area/substantia nigra pars compacta (VTA/SNC) complex. However, both the organization of Acb shell projections to the nigrostriatal neurons innervating the sensorimotor striatum and the synaptic influence exerted by the Acb shell on these neurons remain to be determined. These questions were addressed in the rat using neuroanatomical and electrophysiological approaches. Combined anterograde tracing from the Acb shell with retrograde tracing from the sensorimotor region of the dorsal striatum revealed that labeled fibers from the Acb shell overlap retrogradely labeled nigrostriatal neurons located in the medial SNC and the lateral VTA but avoid the nigrostriatal neurons located laterally. In addition, stimulation of the Acb-shell induced an inhibition of dopaminergic nigrostriatal neurons projecting to the sensorimotor striatal territory. In agreement with the anatomical observations, these responses were observed in nigrostriatal neurons located in the medial SNC and the lateral VTA but not in nigrostriatal neurons located laterally. These data further establish the existence of a functional link between the Acb shell and the sensorimotor striatum via dopaminergic nigrostriatal neurons. The present study also reveals that among the dopaminergic nigrostriatal neurons innervating the sensorimotor striatal territory, only the subpopulation located in the medial SNC and lateral VTA receives an inhibitory input from the Acb shell. This indicates a functional heterogeneity within the population of dopaminergic neurons innervating a given striatal territory.